Abstract
Introduction
Apparent diffusion coefficient (ADC) values in the developing fetus can be used in the diagnosis and prognosis of prenatal brain pathologies. To this end, we measured regional ADC in a relatively large cohort of normal fetal brains in utero.
Methods
Diffusion-weighted imaging (DWI) was performed in 48 non-sedated 3rd trimester fetuses with normal structural MR imaging results. ADC was measured in white matter (frontal, parietal, temporal, and occipital lobes), basal ganglia, thalamus, pons, and cerebellum. Regional ADC values were compared by one-way ANOVA with gestational age as covariate. Regression analysis was used to examine gestational age-related changes in regional ADC. Four other cases of CMV infection were also examined.
Results
Median gestational age was 32 weeks (range, 26–33 weeks). There was a highly significant effect of region on ADC, whereby ADC values were highest in white matter, with significantly lower values in basal ganglia and cerebellum and the lowest values in thalamus and pons. ADC did not significantly change with gestational age in any of the regions tested. In the four cases with fetal CMV infection, ADC value was associated with a global decrease.
Conclusion
ADC values in normal fetal brain are relatively stable during the third trimester, show consistent regional variation, and can make an important contribution to the early diagnosis and possibly prognosis of fetal brain pathologies.
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References
Righini A, Bianchini E, Parazzini C, Gementi P, Ramenghi L, Baldoli C, Nicolini U, Mosca F, Triulzi F (2003) Apparent diffusion coefficient determination in normal fetal brain: a prenatal MR imaging study. AJNR Am J Neuroradiol 24(5):799–804
Schneider JF, Confort-Gouny S, Le Fur Y, Viout P, Bennathan M, Chapon F, Fogliarini C, Cozzone P, Girard N (2007) Diffusion-weighted imaging in normal fetal brain maturation. Eur Radiol 17(9):2422–2429. doi:10.1007/s00330-007-0634-x
Cannie M, De Keyzer F, Meersschaert J, Jani J, Lewi L, Deprest J, Dymarkowski S, Demaerel P (2007) A diffusion-weighted template for gestational age-related apparent diffusion coefficient values in the developing fetal brain. Ultrasound Obstet Gynecol Off J Int Soc Ultrasound Obstet Gynecol 30(3):318–324. doi:10.1002/uog.4078
Manganaro L, Perrone A, Savelli S, Di Maurizio M, Maggi C, Ballesio L, Porfiri LM, De Felice C, Marinoni E, Marini M (2007) Evaluation of normal brain development by prenatal MR imaging. Radiol Med 112(3):444–455. doi:10.1007/s11547-007-0153-5
Huppi PS, Maier SE, Peled S, Zientara GP, Barnes PD, Jolesz FA, Volpe JJ (1998) Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44(4):584–590. doi:10.1203/00006450-199810000-00019
Neil JJ, Shiran SI, McKinstry RC, Schefft GL, Snyder AZ, Almli CR, Akbudak E, Aronovitz JA, Miller JP, Lee BC, Conturo TE (1998) Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology 209(1):57–66. doi:10.1148/radiology.209.1.9769812
Tanner SF, Ramenghi LA, Ridgway JP, Berry E, Saysell MA, Martinez D, Arthur RJ, Smith MA, Levene MI (2000) Quantitative comparison of intrabrain diffusion in adults and preterm and term neonates and infants. AJR Am J Roentgenol 174(6):1643–1649. doi:10.2214/ajr.174.6.1741643
Miller SP, Vigneron DB, Henry RG, Bohland MA, Ceppi-Cozzio C, Hoffman C, Newton N, Partridge JC, Ferriero DM, Barkovich AJ (2002) Serial quantitative diffusion tensor MRI of the premature brain: development in newborns with and without injury. J Magn Reson Imaging JMRI 16(6):621–632. doi:10.1002/jmri.10205
Hoffmann C, Grossman R, Bokov I, Lipitz S, Biegon A (2010) Effect of cytomegalovirus infection on temporal lobe development in utero: quantitative MRI studies. Eur Neuropsychopharmacol J Eur Coll Neuropsychopharmacol 20(12):848–854. doi:10.1016/j.euroneuro.2010.08.006
Mailath-Pokorny M, Kasprian G, Mitter C, Schopf V, Nemec U, Prayer D (2012) Magnetic resonance methods in fetal neurology. Semin Fetal Neonatal Med 17(5):278–284. doi:10.1016/j.siny.2012.06.002
Maas LC, Mukherjee P, Carballido-Gamio J, Veeraraghavan S, Miller SP, Partridge SC, Henry RG, Barkovich AJ, Vigneron DB (2004) Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. NeuroImage 22(3):1134–1140. doi:10.1016/j.neuroimage.2004.02.035
Boyer AC, Goncalves LF, Lee W, Shetty A, Holman A, Yeo L, Romero R (2013) Magnetic resonance diffusion-weighted imaging: reproducibility of regional apparent diffusion coefficients for the normal fetal brain. Ultrasound Obstet Gynecol Off J Int Soc Ultrasound Obstet Gynecol 41(2):190–197. doi:10.1002/uog.11219
Vasung L, Huang H, Jovanov-Milosevic N, Pletikos M, Mori S, Kostovic I (2010) Development of axonal pathways in the human fetal fronto-limbic brain: histochemical characterization and diffusion tensor imaging. J Anat 217(4):400–417. doi:10.1111/j.1469-7580.2010.01260.x
Schneider MM, Berman JI, Baumer FM, Glass HC, Jeng S, Jeremy RJ, Esch M, Biran V, Barkovich AJ, Studholme C, Xu D, Glenn OA (2009) Normative apparent diffusion coefficient values in the developing fetal brain. AJNR Am J Neuroradiol 30(9):1799–1803. doi:10.3174/ajnr.A1661
Ramenghi LA, Martinelli A, De Carli A, Brusati V, Mandia L, Fumagalli M, Triulzi F, Mosca F, Cetin I (2011) Cerebral maturation in IUGR and appropriate for gestational age preterm babies. Reprod Sci 18(5):469–475. doi:10.1177/1933719110388847
Weidenheim KM, Epshteyn I, Rashbaum WK, Lyman WD (1993) Neuroanatomical localization of myelin basic protein in the late first and early second trimester human foetal spinal cord and brainstem. J Neurocytol 22(7):507–516
Weidenheim KM, Bodhireddy SR, Rashbaum WK, Lyman WD (1996) Temporal and spatial expression of major myelin proteins in the human fetal spinal cord during the second trimester. J Neuropathol Exp Neurol 55(6):734–745
Huppi PS, Dubois J (2006) Diffusion tensor imaging of brain development. Semin Fetal Neonatal Med 11(6):489–497. doi:10.1016/j.siny.2006.07.006
Marks MP, de Crespigny A, Lentz D, Enzmann DR, Albers GW, Moseley ME (1996) Acute and chronic stroke: navigated spin-echo diffusion-weighted MR imaging. Radiology 199(2):403–408. doi:10.1148/radiology.199.2.8668785
Desai V, Shen Q, Duong TQ (2012) Incorporating ADC temporal profiles to predict ischemic tissue fate in acute stroke. Brain Res 1458:86–92. doi:10.1016/j.brainres.2012.04.004
Kralik SF, Taha A, Kamer AP, Cardinal JS, Seltman TA, Ho CY (2013) Diffusion imaging for tumor grading of supratentorial brain tumors in the first year of life. AJNR Am J Neuroradiol. doi:10.3174/ajnr.A3757
Barajas RF Jr, Rubenstein JL, Chang JS, Hwang J, Cha S (2010) Diffusion-weighted MR imaging derived apparent diffusion coefficient is predictive of clinical outcome in primary central nervous system lymphoma. AJNR Am J Neuroradiol 31(1):60–66. doi:10.3174/ajnr.A1750
Viola A, Confort-Gouny S, Schneider JF, Le Fur Y, Viout P, Chapon F, Pineau S, Cozzone PJ, Girard N (2011) Is brain maturation comparable in fetuses and premature neonates at term equivalent age? AJNR Am J Neuroradiol 32(8):1451–1458. doi:10.3174/ajnr.A2555
Carson MJ, Thrash JC, Walter B (2006) The cellular response in neuroinflammation: the role of leukocytes, microglia and astrocytes in neuronal death and survival. Clin Neurosci Res 6(5):237–245. doi:10.1016/j.cnr.2006.09.004
van der Voorn JP, Pouwels PJ, Vermeulen RJ, Barkhof F, van der Knaap MS (2009) Quantitative MR imaging and spectroscopy in congenital cytomegalovirus infection and periventricular leukomalacia suggests a comparable neuropathological substrate of the cerebral white matter lesions. Neuropediatrics 40(4):168–173. doi:10.1055/s-0029-1243228
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We declare that all human and animal studies have been approved by the Institutional Review Board and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. We declare that patient consent was waived in this study.
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We declare that we have no conflict of interest.
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Chen Hoffmann and Boaz Weisz contributed equally to the manuscript.
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Hoffmann, C., Weisz, B., Lipitz, S. et al. Regional apparent diffusion coefficient values in 3rd trimester fetal brain. Neuroradiology 56, 561–567 (2014). https://doi.org/10.1007/s00234-014-1359-6
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DOI: https://doi.org/10.1007/s00234-014-1359-6